Reference: Biol. Bull. 192:243-252. (April, 1997)

Morphology and Development of Odostomia columbiana Dall and Bartsch (): Implications for the Evolution of Gastropod Development

RACHEL COLLIN1 * AND JOHN B. WISE2 1 Department of Zoology, University of Washington, Box 351800, Seattle, Washington 98195; and 2 Houston Museum of Natural Science, 1 Herman Circle Drive, Houston, 77030

Abstract. Although pyramidellid gastropods are a phy- plaining the evolution of gastropod cleavage type and logenetically important group of diverse and abundant larval heterochrony. Unequal cleavage and larvae that ectoparasites, little is known about their life histories. hatch without well-developed eyes and tentacles may be Herein, we describe the adult morphology and develop- characteristic of the common ancestor of pyramidellids ment of the pyramidellid Odostomia columbiana, which and opisthobranchs; however, late development of the parasitizes the scallops Chlamys hastata and C. rubida larval heart is probably a derived condition of opistho- in the Northeast Pacific. Anatomically, adult O. colum- branchs. biana resemble other known pyramidellids although they lack the tentacular pads typical of other Odostomia Introduction . Embryonic development is similar to that de- Pyramidellids are common ectoparasites in many ma- scribed for other pyramidellids: cleavage is unequal, gas- rine communities, but little is known about their biology trulation is partially by invagination, and considerable and life histories (Haszprunar, 1988; Wise, 1996). In par- growth occurs before hatching. However, embryonic and ticular, data concerning their development and larval bi- larval development are much slower than for other de- ology are lacking. As in many benthic marine inverte- scribed species. The planktotrophic larvae hatch after brates with limited adult dispersal, the duration of a 19 days of intracapsular development and metamor- planktonic larval stage may be a key factor influencing phose about 2 months later. O. columbiana veligers have pyramidellid distribution and population dynamics. a large black pigmented mantle organ to the right of the Long-lived planktonic stages may increase colonization midline, a distinct metapodial tentacle, and three or four of patchily distributed hosts, whereas species that hatch long bristles that project over the operculum from be- as crawling juveniles may have lower probabilities of lo- hind the foot. Observations of newly metamorphosed ju- cal extinction (Thorson, 1950; White et al, 1984; Gum- veniles suggest that previous disagreements regarding the ming, 1993). Therefore, knowledge of pyramidellid de- development of heterostrophy are due to variation in the velopment and larval biology is key to understanding degree of heterostrophy among species. Our observa- their life histories and host-parasite interactions, and to tions also generally corroborate certain scenarios ex- planning effective pest-control strategies for aquaculture. Pyramidellid development is also particularly infor- Received 16 August 1996; accepted 17 December 1996. mative when viewed in a phylogenetic context. Gener- * Address for correspondence: Committee on Evolutionary Biology, ally, pyramidellids are placed, with other families in the Culver Hall, 1025 E. 57th Street, Chicago, IL 60637; e-mail: rcollin®- order Heterostropha, at the base of the heterobranch midway.uchicago.edu Abbreviations: PMO = pigmented mantle organ; bp 1 = anterior buc- clade (Haszprunar, 1988). Although the relationships cal pump; bp2 = posterior buccal pump; VCSGL = ventral ciliated among these families are poorly resolved, pyramidellids strip gland. clearly represent basal members of the clade that in-

243 244 R. COLLIN AND J. B. WISE eludes opisthobranchs and pulmonates, and which is the which two or more developmental modes occur in one sister group of the Caenogastropoda (Haszprunar, 1988; species, may be an example of such taxonomic confu- Bieler, 1992; Mikkelsen, 1996). Knowledge of such basal sion. impressa has been reported to have plank- groups can be useful in tracing evolutionary transitions, totrophic development in and lecitho- determining ancestral character states, and testing evolu- trophic development in Texas. However, these popula- tionary scenarios. This knowledge may be particularly tions may not represent the same species (Bouchet, useful in gastropod development, where evidence for ev- 1989). Both small eggs that develop into planktotrophic olutionary scenarios is often available from derived rep- larvae and large eggs with direct development have also resentatives of only a few clades. For example, van den been reported for Brachystomia rissoides in areas of Biggelaar (1996) found a trend in cleavage type and D- different salinities in Europe (Pelseneer, 1914; Rasmus- quadrant specification from equal cleavage and late spec- sen, 1944, 1951; Thorson, 1946). ification in "archaeogastropods" to unequal cleavage This paper adds to the data on pyramidellid develop- and early specification in opisthobranchs and pulmo- ment while avoiding the taxonomic confusion of previ- nates. Additionally, Page (1994) suggested that hetero- ous studies by describing both the adult morphology and chronic shifts in gastropod development decelerated the the development of the pyramidellid Odostomia colum- formation of larval and adult structures in opistho- biana Dall and Bartsch, 1907. This new information is branch larvae relative to prosobranchs. These scenarios discussed in the context of the general characteristics of were generated primarily from observations of derived pyramidellid development and its implications for the caenogastropods, opisthobranchs, and pulmonates. evolution of development within the gastropods. Moreover, detailed descriptions of pyramidellid devel- opment could be used to further support or refute these Materials and Methods types of scenarios. To date, accounts of pyramidellid reproduction and Mature Odostomia columbiana were found on the embryology are brief and limited to a small number of scallops Chlamys hastata and C. rubida dredged European (Lebour, 1932, 1936; Rasmussen, 1944,1951; from 90-130 m in San Juan Channel, Washington Fretter and Graham, 1949), eastern North American (48°34'10" N, 123°2'0" W) during March 1995. Both the (Robertson, 1978; White et al., 1985), and Indo-Pacific snails and their hosts were kept at ambient sea tempera- (Amio, 1963;Nishinocfa/., 1983; Gumming, 1993) spe- ture (8°-12°C) in flow-through sea-tables at Friday Har- cies (Table I). Although more than 50 species have been bor Laboratories, Washington. Snails ranged from 5 to reported from western North America (Dall and Bartsch, 8 mm in length and were identified as O. columbiana on 1909), there exists only a single account of pyramidellid the basis of the original description of the shell provided development from the region (LaFollette, 1979). No de- by Dall and Bartsch (1907) and by comparison with the tailed embryological studies of pyramidellids have been holotype and five syntypes on deposit at the National published, and larvae that do not metamorphose imme- Museum of Natural History (lot #126658). Voucher diately after hatching are seldom reared through settle- specimens have been deposited at the Field Museum of ment (see Robertson, 1967, for an exception). Conse- Natural History (FMNH 293334: dry shells; FMNH quently, the details of early development, the duration of 293334: formalin-fixed ). the planktonic period, and the events at metamorphosis have been the subject of much speculation (Thorson, Adult morphology 1946; Fretter tf al, 1982). Adult snails were extracted for dissection by first Published accounts of pyramidellid reproduction and cracking their shells with a vise. Snails were dissected development are often obscured by taxonomic confu- whole, and structures of the gut and reproductive tract sion within the group. Criteria used to identify species were routinely stained with toluidine blue (Wise, 1993, are often not explicitly stated in published reports, or the 1996). is so conjectural that species cannot be identi- fied with much certainty. For example, Clark (1971) and Development Hoffmann (1979) did not state how they identified their snails as Odostomia columbiana, and Cumming (1993) Egg masses were present on the scallops when they was unable to definitely identify "Turbonilla sp." to ge- were collected, and adult snails continued to produce egg nus or species. This taxonomic uncertainty makes it masses in the laboratory until May 1996. Scallop shells difficult to interpret comparative reproductive and de- were checked for new egg masses several times a month velopmental data. to determine whether reproduction was seasonal. Indi- Reports of poecilogony, a rare condition in gastropods vidual egg masses were removed from the scallop shells (Hoagland and Robertson, 1988; Bouchet, 1989) in and kept in small glass dishes while their development TRENDS IN GASTROPOD DEVELOPMENT 245 was observed. Although we did not observe egg laying, several egg masses were collected before the beginning of first cleavage. Observations of these egg masses were used to produce a developmental timetable. Eggs and egg cap- sules were measured prior to first cleavage, and measure- ments were taken in the plane of the chalazae. After hatching, larvae were transferred to filtered (0.45 /xm) seawater in small glass dishes. They were fed Isochrysis galbana and Rhodomonas sp. ad libitum, and the water Figure 1 Diagram of alimentary tract of Odostomia columbiana. was changed every 2 to 3 days. Because the larval shells aes = anterior esophagus, bpl = buccal pump 1, bp2 = buccal pump 2, are hydrophobic, flakes of cetyl alcohol were added to the bs = buccal sac, p = proboscis, pes = posterior esophagus, sb = stylet bulb, sd = salivary gland duct, sgl = salivary gland, su = sucker. Scale surface of the cultures to prevent larvae from becoming bar is 500 pm. trapped in the surface tension. When the veligers began to spend time crawling, juvenile scallops were added to the cultures to induce metamorphosis and as food for hemocoel (Fig. 1). Introvert joining buccal sac (contain- newly metamorphosed juveniles. All observations re- ing buccal sucker, stylet, and stylet bulb), which is con- ported are of animals reared or maintained in the labo- nected to buccal pump. Buccal pump divided into an- ratory. terior (bpl) and posterior (bp2) sections, with bp2 Larval shells were prepared for scanning electron mi- one-third longer than bpl; bpl narrow, round in cross- croscopy by rinsing them in dilute bleach and distilled section; bp2 wider, laterally flattened, distally rounded. water following the procedure of Hickman (1995). They Short, straight anterior esophagus originating on ventral were mounted on stubs with double-sided tape, coated surface of alimentary tract at bpl-bp2 juncture, extend- with gold and palladium, and examined with a JEOL ing posteriorly to join posterior esophagus and paired JM35 scanning electron microscope. salivary glands, forming a four-way junction. Long, highly coiled posterior esophagus extending posteriorly Results to enter visceral mass and join stomach. Long, narrow Adult morphology salivary glands equal to bp2 in length. Salivary gland ducts highly folded and attached to anterior esophagus. The following is given in the concise style of a species Ducts penetrating alimentary tract just anterior to bpl- description. bp2 juncture, extending parallel to one another within Shell: Relatively thin, elongate conical, chalky white, walls of bpl and entering stylet bulb without exiting gut. 5-8 mm in length, composed of 5 to 6 adult whorls. Salivary glands not attached distally to esophagus. Adult whorls with numerous fine spiral growth lines. Pallial Cavity: Mantle and mantle organs typical of Whorl shoulders rounded, with moderately deep sutures. members of the Odostominae, with exception of position Shell etched and pitted, particularly above . of ventral ciliated strip gland (=VCSGL). Small, spheri- Lenticular aperture, with flared lower portion. Single, cal, yellow VCSGL underlying 20% of ventral ciliated short, acute columellar fold on upper half of strip about halfway from anterior edge of mantle floor. perpendicular to columellar axis. Smooth, sinistrally het- Ventral and dorsal ciliated strips joining on mantle roof erostrophic protoconch oriented 130 degrees to teleo- posterior end of mantle cavity. Small, round-to-oblong conch axis, with 40% submerged within first adult whorl. pigmented mantle organ (=PMO), composed primarily Operculum brown, lenticular, with subcentric nucleus. of cells containing a bright yellow exudate, framed by Head-Foot: White to yellow, with numerous scattered numerous brown cells. A thick, bright yellow exudate is white cells. Propodium with slight medial indentation released when snail is disturbed. and rounded lateral edges. Foot narrows posterior to pro- Reproductive System: Opaque-to-transparent repro- podium, then widening to gradually taper to a blunt ductive organs located on columellar side. Common pal- apex. Pedal gland opens in middle of groove extending lial gonoduct extends anteriorly from visceral mass to along posterior half of ventral surface of foot. Attach- open on right side of head just anterior and beneath the ment thread present. Tentacles subtriangular, connate, right tentacle. ventrolaterally folded; tentacular pads apparently ab- sent. Black round eyes beneath epithelium on median Reproduction and development side of tentacles. Mentum unnotched, not bifurcate. Alimentary Tract: Retracted introvert-proboscis ex- Our observations of reproduction and larval develop- tending posteriorly from its aperture on ventral side of ment of O. columbiana generally agree with previous ac- head, dorsal to mentum base and entering cephalic counts of pyramidellid development (Pelseneer, 1914; 246 R. COLLIN AND J. B. WISE

Table I Review ofpyramidellid development

Egg size Capsule size Days to Larval duration Temp. Species (urn) (**m) hatching (days) CQ Reference

Boonea impressa 130* 180-280* 3-5 7 -25 Whiter al., 1985 Brachyslomia rissoides 120 500 25 0 7 Rasmussen, 1951 Brachystomia rissoides 60 200 7 7 7 Thorson, 1946 Brachyslomia rissoides 70 200 6 ? -20 Rasmussen, 1944 Brachystomia rissoides 100 380 25 0 7 Pelseneer, 1914 Chrysallida cincta ? 320 22-27 0 20 LaFollette, 1979 Chrysallida decussata 90-120+ 240-350 7 7 ? Lebour, 1936 diaphana 80* 200 16 ?>8 11 Kristensen, 1970 Odostomia acuta -80* 160X200 a few 7 7 Haisaeter, 1989 Odostomia columbiana 72-74 153-178 19 -70 12 this study Odostomia desimana 80 130 X 160 14 7 7 Amio, 1963 Odostomia eulimoides ? ? 10-12 3-4 18 Fretter and Graham, 1949 Odostomia eulimoides 90* 160 7 7 7 Lebour, 1932 Odostomia fujitaii ? ? 15-16 8-12 15 Minichev, 1971 Odostomia sp. -100* -200* 7 3(?) 22 Nishino etai, 1983 Odostomia omaensis 60 120 X 150 8 7 7 Amio, 1963 Turbonilla sp. 130 300 X 400 10-11 3-5 or 0 23 Gumming, 1993

* Measured from figures. 14-8 eggs per capsule.

Lebour, 1932,1936; Rasmussen, 1944,1951; Fretter and the hosts' shells continually from March 1995 until May Graham, 1949; White et al, 1985). However, both em- 1996 when the last of the snails died. Irregular egg masses bryonic (used here to refer to development prior to are often deposited in groups, making it difficult to dis- hatching) and larval development are much slower than tinguish individual masses. Each snail generally pro- reported for other species (Tables I and II). Although we duced several egg masses per week. searched for spermatophores like those described by Individual eggs are white and range from 71 to 77 /urn Robertson (1978), at no time did we And any attached in diameter (mean = 74.5; SD = 1.61; n = 23). Egg size to the shells or bodies of these snails. Egg masses each did not differ between summer (July) and winter (Janu- containing up to several hundred eggs were deposited on ary). Each round egg, surrounded by an oval layer of opaque albumin, is enclosed in a thick transparent ge- latinous capsule (Fig. 2A-F). The length of the space Table II enclosing the albumin is 154-170 nm (mean = 162.5; SD = 4.6; n = 23) and the outer length of the capsule is Developmental time table for O. columbiana at 10-12°C 193-222 Mm (mean = 211; SD = 6.9; n = 23). In some previous accounts of pyramidellid development (e.g., Age Stage White et al, 1985), capsular length has been reported as ~6h First cleavage egg size, whereas other studies measure the egg cell. In 18h 4 cells this paper "egg" is used to denote the actual egg cell, 24 h 8 cells and "capsule" refers to the egg and the albumin con- 48 h Round blastula 2-3 days Gastrulation: blastula flattens and then forms a tained in one gelatinous covering. The capsules are con- horseshoe-shaped gastrula nected to one another by thin strands called chalazae. In 3-7 days Gastrula O. columbiana, chalazae are composed of a thin extra- 8 days Foot and head rudiments begin to differentiate, some embryonic layer that surrounds the albumin layer be- trochal ciliary motion; the shell is not yet present neath the capsule, traverses the capsule, and continues 10 days Shell, cilia, and foot with operculum and statocysts present, light red PMO just visible between capsules as a thin tubular strand (Fig. 2C). The 17 days Heartbeat and ciliary motion in gut visible egg, albumin, and capsular covering are embedded in a 19 days Veligers hatch, PMO is black transparent gelatinous matrix that is often covered with 72-80 days Veligers begin to crawl diatoms. -90 days Settlement and metamorphosis All eggs within a single egg mass develop synchro- TRENDS IN GASTROPOD DEVELOPMENT 247

Figure 2. Stages in Odosiomia columbiana development. (A) Two-cell stagei (B) four-cell stage; (C) blastula; (D) begining of differentiation of the foot, velum, and shell: (F.) hatch ting veliger; (F) empty egg capsule, In A and B the capsule appears round because il is viewed end on. Chalazae are clearly visible in iheupperrightofCaruJ the upper left of F, All figures are to the same scale, and scale bar is A is 40 mm. nously, and the initial cleavages are simultaneous. First a four-eel! stage with two relatively large cells and two cleavage is clearly unequal (Fig. 2A), but the second small cells (Fig. 2B). Third cleavage is also unequal. Be- cleavage appears to be more-or-less equal. This results in cause the polar bodies are initially obscured by the 248 R COLLIN AND J. B. WISE

Figure 3. Scanning electron micrograph of Odoswmia cohanbiana larval shell at hatching. Apical, apertural. and umbilical views, from left to right. Shell length is 150-160 pm for these three shells.

opaque albumin, the polarity and direction of this divi- points slightly to the 's right when they swim. As sion could not be determined. the loot grows, the metapodial tentacle, the posterior After 2 days the initially spherical blastuia flattens protuberance of the foot (distinct from adult metapodial (Fig. 2C) and in the next few days develops into a heart- tentacles) and its terminal cilia, which extend over the shaped or cup-shaped gastmla. Thus gastrulation occurs operculum, become more obvious. On each side of the at least partially by invagination, as is typical of many foot, three or four bristles, which seem to originate be- opisthobranchs. After 8 days the foot, head, and velum hind the foot, project radially over the edge of the oper- anlangen appear (Fig. 2D), and short cilia present on the culum. Veligers develop eyes within 18-23 days of velar lobes beat weakly. Even after the cilia are fully hatching. After 2 months, the velum shrinks and the lar- formed the embryos rotate very slowly, if at all, within vae, which are about 290 ^m in shell length, begin to the capsules. After 10 days the shell and statocysts are crawl. Larvae at this stage settle and metamorphose clearly visible, and the pigmented mantle organ begins to within days of the addition of juvenile scallops to the cul- develop. As the PMO grows it darkens and changes from ture. Larvae that were the same age but had not begun to dark red to black before the larvae hatch. At 17 days the crawl did not settle in response to scallops. Water in beating heart is visible, and the cilia of the gut arc active. which scallops had been kept overnight did not induce The embryo continues to absorb the surrounding albu- metamorphosis in crawling larvae. The PMO remained min and grows until it eventually fills the capsule. At no dark for at least 1 month after metamorphosis (Fig. 4), time during development did we observe paired larval but had turned yellow after 6 months. kidneys similar to those described by Pelseneer (1914). Additionally, methods used to demonstrate protein up- Discussion take in morphologically similar caenogastropod larval 1 'axonomic note kidneys {Collin, unpubt. data) did not detect protein up- take in decapsulated embryos. Inspection of capsules, af- The snails used in this study were identified as O. co- ter hatching, shows that larvae hatch through an opening lumbiana on the basis of the original description of the in the capsule along one of the chalaza! strands (Fig. 2F). shell (Dall and Bartsch, 1907, 1909) and by comparison At hatching the smooth, sinistral protoconch com- with the type specimens. All animals were collected at- prises nearly an entire whorl (Fig. .V) and is I 50-160 fjm tached to Chlamy.s spp. However, previous papers have in length (n = 7; Fig. 3). Newly hatched larvae have a described O. columhiana found on Trichotropis can- black PMO just to the right of the midline, a small hi- cellata in Puget Sound, but did not state how the snails lobed velum, and no eyes, tentacles, or obvious apical were identified (Clark, 1971; Hoffmann, 1979), Pyrami- tuft (Fig. 2E). Except for the PMO and the stomach and detlid snails on 7 cancellata are much smaller(2-4 mm, digestive gland, whose color reflects larval diet, the veli- pers. obs., RC) than the snails used in this study and ger is entirely transparent. Although larvae retracted into those described by Dall and Bartsch (up to 8 mm). The their shells when placed under the microscope, the foot differences in size and host suggest that these may be two TRENDS IN GASTROPOD DEVELOPMENT 249

vary glands form a four-way junction (Fig. 1). Odo- stomia columbiana, as well as other members of the sub- family Odostominae, will ultimately be relegated to other genera (Wise, in prep.).

Pyramidellid development The reproduction and development of O. columbiana is similar to that previously described for other pyrami- dellids (Lebour, 1932, 1936; Rasmussen, 1944, 1951; Fretter and Graham, 1949; White eta/., 1985), although most of these descriptions are brief and smalt differences may have been overlooked. Eggs of O. columbiana are relatively small, but not unusually so (Table I). Because embryos grow to fill the capsule before hatching, capsule size is a good predictor oflarval size in pyramidellids. O. columbiana deposits a single egg per capsule, as do other pyramidellids except Chrysallida decussala {Table I), Development of O. columbiana is slower than in other species with comparable egg size; only species with large eggs and direct development have a similarly long em- bryonic period (Table 1). Because water temperatures Figure 4. Juvenile Odoatamia columbiana at the edge of a scallop were either not reported or varied considerably in several shell about I month after settlement. The black PMO is visible through previous studies, it is difficult to determine whether these the shell in the middle of the body whorl. Shell length is about 700 ftm. differences in development rate were due to temperature. In O, columbiana the long embryonic period is fol- lowed by an unusually long planktonic larval stage. Al- different species. Nevertheless, the adult shell shape, though times to metamorphosis may be different in the sculpture, protoconch morphology, and adult anatomy laboratory than in nature, veligers in two non-overlapping are quite similar. cultures settled at the same age. Furthermore, recent im- Previous studies have reported that some pyramided provements in larval culture technique and larval diet lids may not be host specific, or their preference may have reduced the time to metamorphosis in cultures of change as they grow (Boss and Merrill, 1965; Powell et other invertebrate larvae (Strathmann, 1987). This sug- ai, 1987), suggesting that the association of small ani- gests that the longer larval period of 0 columbiana in mals with T. cancellaia and large animals with Chlamys comparison to other laboratory-reared pyramidellid spe- spp, may represent an ontogenetic host shift. This is un- cies from previous studies is real (Table I). Unfortunately likely because juvenile O. columbiana raised in this study these studies did not indicate if the larvae studied were did not move onto ']'. cancellaia when given the choice planktotrophic or if food was added to the larval cultures. between juveniles of Chlamys spp, or T. cancellaia. No A distinctive characteristic of the O. columbiana veligers egg masses were discovered on T cancellaia, so it is un- is the presence of bristles extending over the operculum clear whether the pyramidellids from these hosts were from the side of the foot. These are not figured or men- sexually mature. Our preliminary results suggest that tioned in any other description of pyramidellid larvae. these are closely related species. Our observations increase the data on the distribution of several developmental characters that are used in het- erobranch systematic^. Robertson (1985) suggested that Adult morphology chaiazae may be a useful synapomorphy shared by pyra- The morphology of O columbiana is very similar to midellids, architectonicids, and opisthobranchs. Chaia- that of other members of the family. However, it differs zae are clearly present in egg masses of O. columbiana in several ways from the morphology of known species and many other pyramidellids. HeisaUer (1989), how- of the Odostomia. Odostomia columbiana lacks ever, suggests that some pyramidellids lack chala/ae and tentacular pads, and its gut arrangement issimiiartothat that their presence may be a useful systematic character found in members of the genus Boonea except that the within the pyramidellids. He did not find chaiazae in O. salivary gland ducts are attached to the anterior esopha- acuta, and they were not mentioned in descriptions of gus, which with the posterior esophagus and paired sali- egg masses from Brachystomla eulimoides (Lebour, 250 R. COLLIN AND J. B. WISE 1932) and Odostomia sp. (Nishino et al., 1983). Addi- veal several trends in gastropod development. Among tionally, the shape and thickness of the chalazae of O. gastropods there is a trend in both caenogastropods and fujitanii figured by Minichev (1971) are clearly different opisthobranchs toward unequal cleavage and early D- from those in O. columbiana and other pyramidellids. quadrant specification (Freeman and Lundelius, 1992; Spermatophores have also been used as a systematic van den Biggelaar, 1996; van den Biggelaar and Hasz- character within pyramidellids to define the genus prunar, 1996). Equal cleavage with 4d cell formation at Boonea (Robertson, 1978). O. columbiana apparently the 64-cell stage as in "archaeogastropods" is assumed to lacks spermatophores; however, this character has been be the ancestral condition. In opisthobranchs, the first observed in some other species occurring in the north- one or two cleavages are unequal, and the 4d cell is pro- eastern Pacific (A. J. Kohn, pers. comm.). duced by the 24-cell stage. Intermediate conditions occur Our observations of pyramidellid development from in the Architaenioglossa and the Valvatoidea, and there hatching to metamorphosis illuminate several points is considerable variation in basal opisthobranchs (van that have been the subject of much conjecture. At hatch- den Biggelaar, 1996). Although Pelseneer (1914) and van ing, veligers of O. columbiana are morphologically sim- den Biggelaar and Haszprunar (1996, citing Pelseneer) ilar to veligers of other planktotrophic pyramidellid spe- report equal cleavage in pyramidellids, first cleavage in cies, all of which seem to have small, nonpigmented ve- O. columbiana is clearly not equal. In addition, White et lums. Previous studies that failed to rear larvae to al. (1985) figured an unequal two-cell stage of Boonea metamorphosis often concluded that the larval period is impressa in the process of division. This suggests that ei- short because the velum is small {e.g., Thorson, 1946). ther cleavage varies among pyramidellids (an unusual This is not the case for O. columbiana, which has a long occurrence in gastropod groups) or Pelseneer's account planktonic period during which its velum remains small. is inaccurate. Regardless, it is interesting that early cleav- Small velar lobes are also typical of planktotrophic opis- age divisions in pyramidellids are similar to those in an- thobranch larvae (pers. obs., RC), although caenogastro- aspideans and some other opisthobranchs. pods with long-lived feeding larvae often have large com- Page (1994) suggested that heterochronic shifts in the plex velar lobes (Thorson, 1946). timing of development of larval and adult organs ac- Confusion exists as to how differential shell growth count for some of the variation in gastropod larval devel- around the aperture results in heterostrophy (the change opment. In "archaeogastropods" the adult organs de- of coiling direction from a left-handed protoconch to a velop directly from the embryo, whereas in caenogastro- right-handed teleoconch). Thorson (1946) illustrated pods the larva hatches with well-formed larval organs several pyramidellid shells near metamorphosis and and subsequently develops the definitive adult struc- stated that the outer apertural margin of the larval shell tures. Development is retarded in opisthobranchs, and thickens to become a new columella at metamorphosis. they hatch at a stage of morphogenesis similar to that of Fretter et al. (1982) disagreed and suggested that the pro- unhatched caenogastropods: some larval organs develop toconch's outer lip is continuous with the outer lip of the after hatching, and the definitive adult organs develop teleoconch. In O. columbiana, the position of the colu- during late larval life or at metamorphosis (Page, 1994). mella shifts clockwise around the aperture as the coiling Page (1994) paid particular attention to the stage of for- direction changes, but not to the extent described by mation of the eyes, tentacles, and larval heart. Caenogas- Thorson (1946). These conflicting observations of tropod veligers hatch with well-formed eyes and tenta- changes in shell shape at metamorphosis may be due to cles, and the larval heart develops long before hatching variation in degree of heterostrophy among pyramidellid (Page, 1994, and pers. obs). In opisthobranchs, the larvae species. Although the coiling direction reverses in all hatch before the eyes or tentacles have formed, and the cases, there is considerable variation in the displacement larval heart usually forms during the last half of the of the coiling axis of the teleoconch relative to that of the planktonic stage (Page, 1994). The observations of O. co- protoconch. In most of the species figured by Thorson lumbiana reported here suggest that pyramidellid larval (1946), the protoconch is offset roughly perpendicular to development may combine characters of opisthobranch the teleoconch. However, in O. columbiana and and caenogastropod development. As in opisthobranchs, Brachystomia eulimoides (one species studied by Fretter the eyes and tentacles did not appear until well into larval and Graham, 1949), the angle between the coiling axes development; as in caenogastropods, the heart began to of the protoconch and teleoconch often appears to be beat well before hatching. closer to 140 degrees (Fretter £/ al, 1982). These observations support recognized trends in the evolution of gastropod development and suggest ances- Evolution of gastropod development tral character states. Unequal cleavage is characteristic of Detailed studies of embryology and larvae of "archae- pyramidellids and some basal opisthobranchs, whereas ogastropods," caenogastropods, and opisthobranchs re- caenogastropods have a polar lobe; thus unequal cleav- TRENDS IN GASTROPOD DEVELOPMENT 251 age may be a heterobranch synapomorphy. However, Oregonian faunal area. Proc. U. S. Natl. Mus. 33:491-534. additional groups at the base of this clade must be exam- Dall, W. H., and P. Bartsch. 1909. A monograph of west American ined to rule out parallel evolution of unequal cleavage pyramidellid mollusks. Bull. U. S. Natl. Mus. 68: 1-258. Freeman, G., and J. W. Lundelius. 1992. Evolutionary implications from an equally cleaving ancestor, because many other of the mode of D quadrant specification in coelomates with spiral opisthobranchs and pulmonates have equal cleavage. cleavage. J. Evol. Biol. 5:205-247. Additionally, larvae that hatch before the development Fretter, V. M., and A. Graham. 1949. The structure and mode of life of eyes and tentacles were probably ancestral for pyrami- of the Pyramidellidae, parasitic opisthobranchs. J. Mar. Biol. Assoc. dellids and opisthobranchs. On the other hand, early ap- U.K. 28:493-532. pearance of the larval heart relative to hatching in pyra- Fretter, V. M., A. Graham, and E. B. Andews. 1982. The proso- branch molluscs of Britain and Denmark. Part 9—Pyramidellidae. midellids and caenogastropods suggests that late devel- J. Moll. Stud. Suppl. 11: 363-434. opment of the heart is a derived feature of the Haszprunar, G. 1988. On the origin and evolution of major gastropod opisthobranchs. It is clearly necessary to have detailed groups, with special reference to the Streptoneura. J. Moll. Stud. 54: descriptions of more phylogenetically intermediate 367-441. groups and to formulate robust phylogenetic hypotheses Hickman, C. S. 1995. Asynchronous construction of the protoconch/ teleoconch boundary: evidence for staged metamorphosis in a ma- before any firm conclusions regarding the evolution of rine gastropod larva. Invertebr. Biol. 114:295-306. these characters can be drawn. Hoagland, K. E., and R. Robertson. 1988. An assessment of poecilo- gony in marine invertebrates: phenomenon or fantasy? Biol. Bull. 174: 109-125. Acknowledgments Hoffmann, D. L. 1979. An attachment structure in an epiparasitic gastropod. Veliger 22: 75-77. We thank A. Kabat (US National Museum of Natural Heisseter, T. 1989. Biological notes on some Pyramidellidae (Gastro- History) for lending us the type specimens of O. colum- poda: Opisthobranchia) from Norway. Sarsia 74:283-297. biana, R. Bieler (Field Museum of Natural History, Chi- Kristensen, J. H. 1970. Fauna associated with the sipunculid Phas- cago) for accepting the voucher specimens, E. 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